Cited by 232Diet, Metabolism, and DiseaseLipid metabolism and disordersEstrogen and related hormone effects

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Monosaccharide-induced lipogenesis regulates the human hepatic sex hormone–binding globulin gene

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Selva, David M., Hogeveen, Kevin N., Innis, Sheila M., Hammond, Geoffrey L.·2007·Journal of Clinical Investigation

DOI 10.1172/jci32249PMC PMC2066187

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Abstract

The liver produces plasma sex hormone-binding globulin (SHBG), which transports sex steroids and regulates their access to tissues. In overweight children and adults, low plasma SHBG levels are a biomarker of the metabolic syndrome and its associated pathologies. Here, we showed in transgenic mice and HepG2 hepatoblastoma cells that monosaccharides (glucose and fructose) reduce human SHBG production by hepatocytes. This occurred via a downregulation of hepatocyte nuclear factor-4alpha (HNF-4alpha) and replacement of HNF-4alpha by the chicken OVA upstream promoter-transcription factor 1 at a cis-element within the human SHBG promoter, coincident with repression of its transcriptional activity. The dose-dependent reduction of HNF-4alpha levels in HepG2 cells after treatment with glucose or fructose occurred in concert with parallel increases in cellular palmitate levels and could be mimicked by treatment with palmitoyl-CoA. Moreover, inhibition of lipogenesis prevented monosaccharide-induced downregulation of HNF-4alpha and reduced SHBG expression in HepG2 cells. Thus, monosaccharide-induced lipogenesis reduced hepatic HNF-4alpha levels, which in turn attenuated SHBG expression. This provides a biological explanation for why SHBG is a sensitive biomarker of the metabolic syndrome and the metabolic disturbances associated with increased fructose consumption.

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“This decrease in HNF4α consequently reduces SHBG synthesis and hence the levels of circulating SHBG, resulting in an increase in free testosterone levels (Selva et al. 2007) (Fig.”
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“However, in recent years, in vitro studies showed that under more physiological conditions, insulin did not regulate SHBG production in HepG2 cells [11, 35], as well as in vivo study, using hSHBG transgenic mice, showed that insulin did not downregulate SHBG level either [11].”
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“[47, 48, 50–52].”
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“[20] Futhermore, monosaccharide-induced lipogenesis reduces hepatocyte nuclear factor-4-alpha (HNF4A) levels, which in turn attenuates SHBG expression, and it can be noted that this provides a biologic explanation for the sensitivity of SHBG as a biomarker of the metabolic syndrome.[34] In pathological conditions, a p…”
Background
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BackgroundInfluential
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“Several studies (Simó et al., 2012a; Simó et al., 2014; Selva et al., 2007; Simó et al., 2015) have identified HNF-4α as a key factor promoting SHBG synthesis; the HNF4α level in the liver was positively correlated with SHBG levels in the current study.”
Background
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“As we previously reported liver steatosis induces upregulation of PPARγ and downregulation of HNF‐4α levels, both leading to a reduction of SHBG production by the liver (Selva et al., 2007).”
BackgroundInfluentialSelf-citation
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Background
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Background
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“44 This established relationship between SHBG and GDM from those studies formed the basis for which serum SHBG was suggested as a valuable tool for the prediction, diagnosis, and monitoring of GDM. Serum SHBG level was an excellent diagnostic indicator of GDM in the study population with an area…”
Method
Association between sex hormone levels and abnormal metabolism in a population of elderly Chinese men
Gong, Y., Xiao, H., Bai, J., Li, C., Wen, X., Cheng, X., Fu, S., Lu, Y., Li, X., Shao, Y., et al. (2013) · The Aging Male · doi:10.3109/13685538.2013.765402 · Cited by 5
“Some researchers believe that lipogenesis induced by glucose or free fatty acids (in overweight and obesity) inhibits hepatic SHBG expression by reducing cellular HNF-4 levels [24].”
Background
An insight of association of insulin resistance with polycystic ovary syndrome
Basu, B. R., Chakraborty, S., Samaddar, A., Das, N., & Saha, S. K. (2021) · Indian Journal of Clinical Anatomy and Physiology · doi:10.18231/j.ijcap.2021.055 · Cited by 8
Do Dietary Modifications Made Prior to Pubertal Maturation Have the Potential to Decrease Obesity Later in Life? A Developmental Perspective
Casazza, K., & Affuso, O. (2009) · ICAN Infant Child & Adolescent Nutrition · doi:10.1177/1941406409348917 · Cited by 4
Sex Hormone-Binding Globulin and Metabolic Syndrome in Children and Adolescents: A Focus on Puberty
Aydın, B. K., & Winters, S. J. (2025) · Metabolites · doi:10.3390/metabo15080494 · Cited by 4
“These results were called into question, however, as later studies also using HepG2 cells found no effect of insulin on SHBG secretion or mRNA levels, which instead were reduced by adding glucose or fructose to the culture media [7] and by rosiglitazone [115].”
Gonadal hormones and metabolic syndrome in middle-aged and elderly males: results from a prospective cohort study in China
Zhang, Z., Chen, Y., Li, N., Huang, C.-L., Lin, D.-Z., Wang, C.-Z., Wang, C.-Y., You, L.-L., Li, L.-L., Li, F.-P., et al. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1365283 · Cited by 4
“HNF-4 a levels affect the transcriptional activity and synthesis of SHBG. Monosaccharides reduce HNF-4 a levels by directing adipogenesis, reducing SHBG synthesis; therefore, HNF-4 a levels are reduced in overweight and obese individuals, suppressing hepatic SHBG expression (29).”
Background
A Longitudinal Retrospective Observational Study on Obesity Indicators and the Risk of Impaired Fasting Glucose in Pre- and Postmenopausal Women
Nam, M. J., Kim, H., Choi, Y. J., Cho, K.-H., Kim, S. M., Roh, Y. K., Han, K., Jung, J., Park, Y. G., Park, J., et al. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11102795 · Cited by 5
“Increased adiposity could also induce the suppression of hepatic SHBG synthesis, [33,36] and SHBG levels in postmenopausal women are negatively correlated with visceral fat [37].”
Background
Serum Sex Hormone Binding Globulin Concentration as a Predictor of Ovarian Response During Controlled Ovarian Hyperstimulation
Zhai, J., Li, S., Zhu, Y., Sun, Y. W., Chen, Z., & Du, Y. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.719818 · Cited by 4
Association of sex hormone binding globulin with gestational age and parity in gestational diabetes mellitus
Siddiqui, K., George, T., Joy, S. S., & Nawaz, S. (2020) · Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2020.1757059 · Cited by 4
“and further confirmation through in vivo studies indicating a negative association between SHBG and fasting glycemia [20,21].”
Low Levels of Sex Hormone-Binding Globulin Constitute an Independent Risk Factor for Arterial Stiffness in Korean Women
Han, K., Chun, H., Kim, M. J., Cho, D., Lee, S.-H., Won, B. Y., Kim, K., Joo, N., & Kim, Y. (2017) · International Journal of Endocrinology · doi:10.1155/2017/6956495 · Cited by 4
“However, according to recent studies, insulin may not regulate the production of SHBG [33, 34].”
Background
Relationship between testosterone, sex hormone binding globulin, angiopoietin related growth factor and insulin resistance in normal weight and obese men
Mohasseb, M., Nour, H. A., El-Sawaf, A., & Khalil, G. I. (2013) · Alexandria Journal of Medicine · doi:10.1016/j.ajme.2013.10.004
“It was also suggested that excess monosaccharide consumption and levels of fasting glucose rather than elevated insulin levels are the actual determinants of liver SHBG production.36,37 In addition, Selva et al.36, have previously described the role of de novo lipogenesis in the down regulation of hepatic SHBG express…”
Background
Plasma Levels of Sex Hormone-binding Globulin, Corticosteroid-binding Globulin and Cortisol in Overweight Subjects who Develop Impaired Fasting Glucose: A 3-Year Prospective Study
Lewis, J., Shand, B., Frampton, C., Elder, P., & Scott, R. (2008) · Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme · doi:10.1055/s-0028-1087190 · Cited by 4
The predictive value of the metabolic score for insulin resistance for metabolism-related disorders and fertility outcomes in Chinese women with polycystic ovary syndrome
Lu, F., Yu, H., Shi, B., Feng, J., Liu, Y., Guan, M., Yu, J., Gao, Z., Gao, J., Ma, H., et al. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1716287 · Cited by 4
A Mendelian randomization study: Genetically predicted dopamine 4-sulfate to dopamine 3-O-sulfate ratio mediates the association between chemokine C-C motif ligand 11 and polycystic ovary syndrome
Chen, Y., Cao, P., & Li, J. (2025) · Medicine · doi:10.1097/md.0000000000044448 · Cited by 4
“[30] Furthermore, insulin inhibits the activity of insulin-like growth factor binding protein 1 while simultaneously elevating the availability of insulin-like growth factor 1.”
The influence of body composition on the response to dynamic stimulation of the endocrine pituitary-testis axis
Abildgaard, J., Bang, A. K., Nordkap, L., Priskorn, L., & Jørgensen, N. (2024) · International Journal of Obesity · doi:10.1038/s41366-024-01518-2 · Cited by 4
“Thus, obesity, particularly central obesity and steatosis, inhibits production of sex hormone binding globulin (SHBG) [4, 5] contributing to lower circulating total T, through a lower T binding capacity, with only little affection of the free testosterone (FT) concentration [5].”
Background
Examining the associations between testosterone and biomarkers as men age
Smith, S. J., Bekele, D., Lopresti, A. L., & Fairchild, T. J. (2023) · American Journal of Human Biology · doi:10.1002/ajhb.23942 · Cited by 4
Short-time intensive insulin therapy upregulates 3 beta- and 17 beta-hydroxysteroid dehydrogenase levels in men with newly diagnosed T2DM
Hu, Y., Wang, Y., Cai, T., Liu, L., Li, D. M., Ma, J., & Ding, B. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.894743 · Cited by 4
The Cutoff Value of Low Sex Hormone-Binding Globulin and Its Predictive Role in Impaired Glucose Metabolism Among Chinese Women with Polycystic Ovarian Syndrome
Ding, M., Liu, Y., Yang, Y., Ye, Y., Li, L., Huang, J., Chen, X., Yang, D., & Zhao, X. (2021) · Metabolic Syndrome and Related Disorders · doi:10.1089/met.2020.0071 · Cited by 2
“1 Several in vitro 2 and in vivo 3 studies have implicated insulin as a suppressor of hepatic production of SHBG.”
Influential
Excessive amount of lactose in the diet of two-week-old calves inducesurinary protein changes
Dratwa-Chałupnik, A., Ożgo, M., Lepczynski, A., Herosimczyk, A., & Michałek, K. (2016) · Archives animal breeding/Archiv für Tierzucht · doi:10.5194/aab-59-417-2016 · Cited by 3
“Selva et al. (2007) demonstrated that glucose, sucrose and fructose reduced SHBG production by hepatocytes.”
Background
Functional characterization of sex hormone-binding globulin genetic polymorphism
Wu, T.-S. (2015) · cIRcle (University of British Columbia) · doi:10.14288/1.0166338 · Cited by 3
“decrease in HNF4 levels, so that COUP-TF1 can replace it and reduce SHBG production in HepG2 cells (72).”
Background
Metabolic benefits of ketohexokinase inhibition in individuals with MASLD: a randomized placebo-controlled crossover trial
Koene, E., Schrauwen‐Hinderling, V. B., Basset‐Sagarminaga, J., Brouwers, K., Bruls, Y. M. H., Mevenkamp, J., Haans, F., Schaart, G., Moonen‐Kornips, E., Jörgensen, J. A., et al. (2026) · Nature Metabolism · doi:10.1038/s42255-026-01626-5 · Cited by 2
“These hepatokines have a strong mechanistic link with either DNL (that is, SHBG) or its regulators (that is, FGF-21 and follistatin) 25–29 (Fig.”
Ketosis suppression and ageing (KetoSAge): the effect of suppressing ketosis on SHBG and sex hormone profiles in healthy premenopausal women, and its implications for cancer risk and therapy
Cooper, I. D., Petagine, L., Soto-Mota, A., Duraj, T., Seyfried, T. N., Lee, D. C., Cooper, N., & Kyriakidou, Y. (2026) · Frontiers in Nutrition · doi:10.3389/fnut.2025.1731915 · Cited by 2
“…have been consistently associated with elevations in SHBG, accompanied by improvements in glycaemic regulation, insulin sensitivity, and androgen homeostasis (18, 29–32 , 68 Frontiers in Nutrition 16 frontiersin.org generation and simultaneously inhibits SHBG synthesis within the liver (16, 34–36).”
Divergent fat deposition in PCOS: A preliminary comparative analysis of pancreatic and hepatic steatosis in aging clinical and unselected populations
Aksun, S., Eroğlu, B. Ç., Güneşli, I., İdilman, İ. S., Karçaaltıncaba, M., & Yıldız, B. O. (2025) · Maturitas · doi:10.1016/j.maturitas.2025.108810 · Cited by 3
Plasma SHBG Levels as an Early Predictor of Response to Bariatric Surgery
Gabriel-Medina, P., Ferrer, R., Rodríguez‐Frias, F., Comas, M., Vilallonga, R., Ciudin, A., & Selva, D. M. (2024) · Obesity Surgery · doi:10.1007/s11695-023-06981-w · Cited by 3
“The role of SHBG as a biomarker associated with metabolic dysregulation has been described in experimental animal models, which have shown that glucose-and fructose-induced lipogeneses decrease liver SHBG synthesis [13].”
BackgroundSelf-citation
Fructose intake from sugar-sweetened beverages is associated with a greater risk of hyperandrogenism in women: UK Biobank cohort study
Chen, H., Buziau, A. M., Rentería, M. E., Simons, P. I. H. G., & Brouwers, M. C. G. J. (2024) · European Journal of Endocrinology · doi:10.1093/ejendo/lvae006 · Cited by 5
FGF21 Is Released During Increased Lipogenesis State Following Rapid-Onset Radioiodine-Induced Hypothyroidism
Szczepańska, E., Glinicki, P., Zgliczyński, W., Slowinska-Srzednicka, J., Jastrzębska, H., & Gietka‐Czernel, M. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.900034 · Cited by 3
“It has been demonstrated that enhanced de novo lipogenesis in the liver, a process consisting of conversion of acetyl-coenzyme A to free fatty acids, is crucial for NAFLD development and can down regulate SHBG synthesis (44, 45).”
Association of central obesity with sex hormonebinding globulin: a cross-sectional study of 1166 Chinese men
Liu, F.-W., Shen, X., Wang, R., Yu, N. H., Shi, Y., Xiong, S., Xiong, C., & Zhou, Y. (2018) · Open Medicine · doi:10.1515/med-2018-0030 · Cited by 3
Young, healthy South Asians have enhanced lipogenic sensitivity to dietary sugar
Hudgins, L. C., Hugo, J. L., Enayat, S., Parker, T. S., Artis, A. S., & Levine, D. M. (2016) · Clinical Endocrinology · doi:10.1111/cen.13293 · Cited by 2
Association of the (TAAAA)n repeat polymorphism of SHBG gene with the age at menopause in Greek postmenopausal women
Markatseli, A. E., Hatzi, E. G., Pamporaki, C., Bouba, I., Xita, N. V., Tigas, S. K., Georgiou, I. A., & Tsatsoulis, A. A. (2014) · Maturitas · doi:10.1016/j.maturitas.2014.03.009 · Cited by 2
SEX HORMONE BINDING GLOBULIN GENE POLYMORPHISM AND RISK OF TYPE2 DIABETES MELLITUS IN EGYPTIAN MEN
Tarhouny, S. E. E., Zakaria, S., Hadhoud, K. M., Hanafi, M., Kamel, A., & Nozha, O. A. A. (2014) · doi:10.21608/zumj.2014.4372 · Cited by 2
“Hyperinsulinemia induced by insulin resistance probably causes low levels of sex hormone–binding globulin in insulin-resistant conditions such as obesity, type 2 diabetes, and the polycystic ovary syndrome (19) .”
Background
The association between sex hormone-binding globulin and type 2 diabetes in Nigerian men
Abbiyesuku, F. M., Agbakwuru, A. N., & Olawale, O. O. (2013) · African Journal of Laboratory Medicine · doi:10.4102/ajlm.v2i1.44 · Cited by 2
Developmental Programming of Polycystic Ovary Syndrome: Role of Prenatal Androgen Excess
Tsatsoulis, A. A. (2009) · Humana Press eBooks · doi:10.1007/978-1-60327-250-6_5 · Cited by 2
Sex hormone-binding globulin as a context-dependent regulator of sex steroid bioavailability in cancers.
Lee, S. R., & Hong, E.-J. (2026) · Biochimica et biophysica acta. Reviews on cancer · doi:10.1016/j.bbcan.2026.189694 · Cited by 1
Nutrition Across the Life Course and Risk of Young-Onset Breast Cancer: Mechanisms, Evidence, and Prevention Opportunities
Wang, C., & Liu, Z. (2026) · Nutrients · doi:10.3390/nu18122011 · Cited by 1
“High intakes of glucose and fructose inhibit HNF4 α via de novo lipogenesis, while pro-inflammatory cytokines (TNF-α , IL-1 β ) exert parallel repressive effects [176].”
Sex Hormone-Binding Globulin Prevents Carbon Tetrachloride-Induced Liver Fibrosis Development
Álvarez-Guaita, A., Briansó‐Llort, L., Cabrera-Serra, J., Fuertes‐Rioja, L., Ramos‐Perez, L., Salcedo, M. T., Hernández, C., Simó, R., & Selva, D. M. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27114893 · Cited by 1
“Specifically, we and others have shown that SHBG expression is suppressed by (a) hepatic lipid accumulation driven by high-carbohydrate diets [6], (b) elevated levels of pro-inflammatory cytokines such as tumor necrosis factor-alpha (TNF-α ) and interleukin-1 β (IL-1 β ) [9–11], and (c) increased…”
Self-citation
Caloric Restriction Substantially Improves Glucose Regulation in Mice With Hnf1a‐Deficient Beta‐Cells
Sharmine, S., Legøy, T. A., Unger, L., Paulo, J. A., Ghila, L., & Chera, S. (2025) · Acta Physiologica · doi:10.1111/apha.70121 · Cited by 3
“Along the same lines, studies on diabetic patients reported a difference in the mean age of onset of type 2 diabetes based on HNF1A genotype in women, but not in men [56], while also a potential correlation between sex hormones and Hnf1a expression [57] was suggested.”
Chronic high dietary sucrose induces sexually dimorphic metabolic adaptations in liver and adipose tissue
Stephenson, E. J., Stayton, A., Sethuraman, A., Rao, P. K., Gomes, C., Mulcahy, M. C., McAllan, L., Puchowicz, M. A., Pierre, J., Bridges, D., et al. (2020) · bioRxiv · doi:10.1101/2020.05.20.106922 · Cited by 1
“SHBG is thought to interact with ERα to regulate the transport of estrogens (and testosterone) into tissues (Hammond, 2016), and it’s concentrations are negatively associated with the severity of NAFLD and other metabolic disease risk-factors in humans (Kavanagh et al., 2013; Luo et al., 2018).”
BackgroundInfluential
Relatively low sex hormone‐binding globulin concentration is a risk factor for hyperuricemia in middle‐aged Japanese men
Fujihara, Y., Hamanoue, N., Akehi, Y., Motonaga, R., Tanaka, T., Iwaya, C., Yano, H., Tanabe, M., Nomiyama, T., & Yanase, T. (2020) · Obesity Science & Practice · doi:10.1002/osp4.413 · Cited by 1
Sex hormone-binding globulin b expression in the rainbow trout ovary prior to sex differentiation.
Pérez, C., Araneda, C., Estay, F., Díaz, N., & Vizziano-Cantonnet, D. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.11.021 · Cited by 1
The insulin resistance syndrome
Sattar, N. A., Welsh, P. I., & Preiss, D. (2015) · doi:10.1002/9781118387658.ch23 · Cited by 4
Acne
Treloar, V. (2009) · CRC Press eBooks · doi:10.1201/9781420067637.ch20 · Cited by 1
Links Between Polycystic Ovary Syndrome and Gestational Diabetes Mellitus
Trouva, A., & Diamanti‐Kandarakis, E. (2017) · Springer eBooks · doi:10.1007/978-3-319-56440-1_16
REGULATION OF ANDROGEN ACTION BY SEX HORMONE-BINDING GLOBULIN
Hong, E. (2011) · cIRcle (University of British Columbia) · doi:10.14288/1.0105101 · Cited by 1
“It was confirmed that thyroid hormone stimulates SHBG production in cultured HepG2 cells by increasing the steady state of its mRNA concentrations (99, 102), and it is now known that this is an indirect effect mediated by a thyroid hormone-induced increase in hepatic HNF-4α levels (104).”
BackgroundMethodInfluential
Sex Hormone‐Binding Globulin Limits Glucocorticoid‐Induced Muscle Wasting by Preserving Estrogen‐Dependent Repression of Catabolic Signaling
Park, J., Song, A.-Y., Bae, H.-R., Hong, E.-J., & Lee, S. R. (2026) · Acta Physiologica · doi:10.1111/apha.70332

Authors: Selva, D. M., Hogeveen, K. N., Innis, S. M., & Hammond, G. L.
Affiliations: University of British Columbia (CA)
Western University (CA)
Corresponding author: Hammond, Geoffrey L.
ORCID: Selva, David M.
Hogeveen, Kevin N.
Hammond, Geoffrey L.
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2007-11-08
Volume: 117
Issue: 12
Pages: 3979-87
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci32249
PMC: PMC2066187
OpenAlex: W2026196869
Cited by: 232
References: 48
Citations by year: 2026: 9 · 2025: 11 · 2024: 13 · 2023: 14 · 2022: 22 · 2021: 15 · 2020: 12 · 2019: 7 · 2018: 11 · 2017: 20 · 2016: 17 · 2015: 8 · 2014: 9 · 2013: 18 · 2012: 18
FWCI: 4.16
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Child and Family Research Institute
Michael Smith Health Research BC
Canadian Institutes of Health Research
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diet, Metabolism, and Disease
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipid metabolism and disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
Keywords: sex hormone-binding globulin, monosaccharides, glucose, fructose, lipogenesis, HNF4α, promoter cis-acting elements, palmitate, metabolic syndrome, hepatocytes, fructose consumption
MeSH terms: Adult, Animals, Chickens, Child, Child, Preschool, Fructose, Gene Expression Regulation, Glucose, Humans, Mice, Transgenic, Sex Hormone-Binding Globulin, Gonadal Steroid Hormones, Sweetening Agents, Biomarkers, Metabolic Syndrome, Cell Line, Tumor, Lipogenesis, Overweight, Mice, Hepatocyte Nuclear Factor 1-alpha, Hepatocyte Nuclear Factor 4

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Monosaccharide-induced lipogenesis regulates the human hepatic sex hormone–binding globulin gene

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